IPhysiotherapist
 Porto Alegre/RSIIPhysiotherapist and owner of the Acquaticus  Porto Alegre/RS,
Physical Educator, Master in Sciences of the Human Movement  UFRGS, Professor
of the Physiotherapy Course of the PUCRS, Doctorship by the PUCRSIIIPhysiotherapist of the Clube Grêmio Náutico União
 Porto Alegre/RS, Physiotherapist for the Clinica SOS ESPORTE, Master
in Sciences of the Human Movement  UFRGS, Professor of the Physiotherapy
Course of the PUCRS and Unisinos, Doctorship in Sciences of the Human Movement
 UFRGSIVOrthopedics and Traumatology Doctor of the Sports of the Clinica
SOS ESPORTE, Orthopedics and Traumatology Doctor of the Sports and Coordinator
of the Center of Medicine and Rehabilitation for Clube Grêmio Náutico
União Porto Alegre/RS, Medical Director of the Federação
Gaúcha de Futevôlei, and Medical Director for the Federação
Gaúcha de Futebol, Master in Sciences of the Human Movement  UFRGS,
Doctor in Sciences of the Human Movement  UFRGS

The muscular fatigue
(MF) is a common phenomenon in the daily sports activities that results in a
worsening of the motor performance. It is considered one of the major factors
for muscle-skeletal damages, such as the ankle sprain, when the MF would affect
both the afferent and the efferent systems. Several studies have been analyzing
the influence of the MF on the neuromuscular control (NMC). Nevertheless, there
are few researches comprising that influence on the velocity of the muscular
reaction. The purpose of this study was to check the effects of the MF on the
time of the muscular reaction (TMR) in the fibularis muscles, which are the
first to respond to an inversion stress of the ankle. Fourteen healthy male
individuals (age: 20-35 years) were studied, who had their TMR assessed by means
of the surface electromyography (EMG). The beginning of the muscular activity
was defined as the mean resting value +3x the standard deviation (SD). The TMR
of the fibularis was measured after a sudden 20º inversion performed
on a platform. The sudden inversion was performed before and after the muscular
fatigue, which was induced through localized exercises of the fibularis up to
the exhaustion. The results have shown a significant increase in the time of
the muscular reaction after the fatigue (p < 0.01). While performing prolonged
sportive activities and during the rehabilitation process, there must be caution
to perform tasks that require extremely fast muscular responses.

The muscular fatigue (MF) that is defined as any reduction in
the neuromuscular ability to produce strength(1,2) is
a usual phenomenon in resistance sports, and is a common
experience in the daily activities(3). The beginning
of the voluntary muscular activity involves several processes
that start with the cortical control in the brain, and end with
the cross-bridges inside the muscular fiber. Therefore, the
muscular fatigue can be the result of a failure in any process
involved in the muscular contraction(4).

Historically, the potential factors involved in the fatigue
development are divided in two categories: the central factors
that should provoke the fatigue by a disorder in the
neuromuscular transmission between the CNS and the muscular
membrane, and peripheral factors that would cause an alteration
inside the muscle(5-7). Another characteristic of the
fatigue is the fact that it depends on the task, that is, its
causes vary in a very wide way, and it behaves according to the
way it is induced(4,8). The muscular fatigue is
considered a predisposing factor to the appearance of
injuries(9,10), such as the ankle sprain. In the
majority of cases upon the occurrence of such type of injury, the
originator mechanism is an inversion movement of the
ankle(11,12). The responsible by the obstruction in
that harmful stress to the joint is the structure that statically
(fascia, capsule, ligament) and dynamically
(muscles)(13) restricts the joint. The short and
longus fibular muscles are the first and more important
muscular structures that actuate in the prevention of that type
of sprain(14).

Several authors have been studying the effects of the muscular
fatigue on the neuromuscular control (NMC)(9,15-17),
which is related to the proprioceptive afferents that are taken
by the peripheral receptors to the upper centers, and to the
efferent (motor) responses generated with the purpose to keep the
dynamic muscular stability(18). Studies have shown
that the muscular fatigue causes an adverse change in the
proprioception(16,19) (a sensorial modality comprising
the sensations of the joint movement and
positioning(13)), as well as the postural
control(9,15,17,20). However, few studies analyzed the
changes that the muscular fatigue generates in the time of the
muscular reaction (TMR)(3,21,22).

Due to the high incidence of the ankle sprain caused by the
inversion(23,24) and the great amount of occurrences
of the muscular fatigue both in the sportive and daily
activities, and being aware of the major importance that the
effective and fast motor control have to prevent muscle-skeletal
injuries(4), this study had as main purpose to analyze
the effects of the muscular fatigue induced by active-resisted
exercises in the TMR of the fibularis in healthy individuals by
means of surface electromyography (EMG), and to verify if there
is any difference in the EMG activity of the resting fibularis
before and after the muscular fatigue. The fibular reaction was
tested by utilizing a sudden inversion platform.

METHODOLOGY

The research was developed at the Laboratory of the Exercise
Research (LAPEX) of the Rio Grande do Sul Federal University
(UFRGS). Before participating in the study, each individual
granted his formal consent to participate in the research signing
a Free and Clarified Consent Term elaborated following ethic
standards previously approved by the Ethics Committee in Research
of the Rede Metodista de Educação in March,
2004.

Population and sampling

It participated in the study 14 male individual practitioners
of regular physical activity (at least twice a week) with no
previous history of injuries in the lower limbs, and without
compromise in the joint stability of the ankle. All participants
were not performing any physical activity at least 24 hours prior
to the data collection. It was chosen not to use individuals from
both genders because some authors have shown differences between
men and women as to the fatigue(25,26).

Procedures to the data collection

The data collection was performed in three steps: 1)
assessment of the time of the pre-fatigue muscular reaction, 2)
fatigue induction, and 3) assessment of the time of the
post-fatigue muscular reaction. The right lower limb was chosen
to perform the test, regardless the individual's dominance.

To measure the
time of the muscular reaction, it was used a Bortec® electromyograph
(EMG) (Bortec Electronics Incorporation Calgary, Canadá). The EMG had
a 10 cm away from the electrodes preamp, and it was used two channels where
the amplified signal was converted through a digital-analogical board. In order
to record the electromyographic signal, it was used disposable Kendall®
surface electrodes with a 3 cm diameter stick (Meditrace  100; Ag/AgCl)
in the bipolar configuration. To attain the adequate electrode positioning,
each participant was asked to perform a voluntary contraction of the fibular
muscles against manual resistance, in order to allow the identification of the
muscular abdomen, when the electrodes were placed 1/3 below the fibula's head
to fix the electrodes.

Ground electrodes were placed on the tibialis tuberosity of
the left leg, and the skin was shaved using a disposable razor,
in order to reduce the electrical impedance and by scraping the
skin with alcohol-soaked cotton to remove dead cells and the
oiliness at the spot where the electrodes were
positioned(27). Next, the electrodes were fixed on the
skin through a mild pressure in order to increase the contact
area between the electrode's gel and the skin(28).

It was used a 20º sudden ankle inversion platform
with a synchronism system connected to a computer, which was able
to inform the precise moment when the platform would tumble
against the board's base, thus signalizing the end of the
inversion spinning. With no previous warning, the board device
was manually triggered, simulating a sprain by ankle inversion.
At that moment, the computer collected the muscular response from
the fibularis, as well as the moment when it occurred. The same
procedure was performed in two different periods: in the
beginning that is, before the muscular fatigue, and in the end,
after the fatigue. The individual was in orthostatic position on
the board, with his arms interlaced on the thorax, and next, he
was oriented to stare a fixed point at the height of his eyes, in
a way they could not see when the researcher was triggering the
mechanical device of the board. At that moment, the computer was
already collecting the (resting) muscular electrical
activity.

The muscular fatigue was induced through active localized
resisted exercises. The muscular fatigue is defined in the
literature as a failure in the neuromuscular system in its
ability to generate a required or expected
strength(10). When performing voluntary strengths,
such failure can result from several central or peripheral
mechanisms(5).

Thus, the fatigue induction was performed through ankle
eversion exercises against the resistance. The individual was
seat on a little mattress with his backs supported by the wall,
his knees and left hip inflected. The right lower limb was
positioned in a 90º flexion of the hips with extended
knees and the ankle in a neutral position. He was barefoot. By
using a green Theraband® brand elastic band, the
researcher was on the left side of the individual, and he
positioned the elastic band on the external side of the foot,
thus creating a resistance against the eversion movement. The
individuals were instructed to perform the higher amount of
eversions possible, and they always received oral stimuli. Such
Theraband® band was used because it supplies a
medium resistance(30) due to the heterogeneity of the
sampling, and the fact that the electrical capability of the
participants was not previously known. The test was performed in
every individual with the same researcher. Even with the whole
methodological criterion used, it cannot be asserted that every
participant reached the same fatigue level; it can only be
asserted that they achieved some fatigability level that made
them unable to go on performing the task.

After the fatigue induction, the individual was once again
positioned on the board (located 1 meter away the place where the
exercises were performed), and the TMR was measured once again
through a sudden inversion. The post-fatigue measurement occurred
in less than 10 seconds after the muscular fatigue of the
fibularis.

Analysis and filtering of the electromyographic
signals

Initially, a 3-order Butterworth filter was used at a 20-600
Hz frequency. The resting period was considered the prior 2
seconds to the stimulus, from which the mean and the standard
deviation of the resting EMG signal were obtained. From these
data, it was possible to determine the threshold to detect the
muscular activity. This means that the EMG signal that it would
surpass that threshold would be the muscular activation above the
resting. The criterion for the muscular activation was based on
the following calculation: Threshold = mean + (3x SD). Whenever
using three deviations above the mean, the result attained was
99.7% chance to consider a different activity from the
resting(30). To set the time for the reaction of the
fibularis muscles, it was set the moment when the first muscular
activation peak occurred (post-stimulus), when the threshold
would be surpassed. The difference between the moment when the
external stimulus occurred and the activation peak was set as the
time of the muscular reaction, or the time of the
electromyographic response.

Statistical analysis

It was used the t Student test for paired sampling to
compare the resting activity of the fibular muscles before and
after the fatigue, as well as to check the differences in the
time of the pre- and post-fatigue muscular reaction. The
significance level used was p < 0.05.

RESULTS

The characteristics
of the 14 participants are presented on table 1. The
mean age was 25 ± 3.94 years; height: 1.75 ± 0.06 meters; weight:
72.71 ± 11.71 kg; the amount of days they performed physical activities
per week was 4.10 ± 1.60, and the amount of eversion repetitions performed
along the fatigue induction was 113.40 ± 34.60.

The resting electrical
signal (v) (defined as the 2 seconds period before the stimulus) of the fibularis
was higher than in the post-fatigue period (0.031 ± 0.020) compared to
the pre-fatigue values (0.025 ± 0.013). Nevertheless, there was no statistically
significant difference (p > 0.05). Table 2 presents
the values related to each participant.

The comparison
between the fibular TMR in the pre- (68 ± 9.7 ms) and post-fatigue (78
± 7.4 ms) period has shown a statistically significant increase in the
TMR in the post-fatigue period (p < 0.001), as shown on graphic
1.

DISCUSSION

This study aimed to analyze the influence of the muscular
fatigue in the fibular TMR. The sampling was composed by 14 male
individuals. It was chosen not to use individuals from both
genders as some authors have shown differences between men and
women as to the fatigue(25,26). The majority of the
studies performed show that women have higher resistance to the
fatigue during submaximal contractions. One of the goals of the
present study was to check whether there is a difference in the
EMG activity of the resting fibular muscles in the postural
controlling and/or balance(9,15,17,20,32), and in only
one of the studies the muscular fatigue did not cause an adverse
postural change (15). As the postural control is kept
through some afferences that come from the visual, vestibular,
and somatosensory systems that stimulate the continuous muscular
contractions(15,17,20), and as the muscular fatigue
changes the muscular contractile effectiveness and proprioceptive
information(15,16,32,42), these results are not
surprising.

In order to keep the balance in the orthostatic positioning
according to the individuals' positioning along the data
collection, it is necessary constant corrective contractions as a
response to the small disturbances in the joint(20).
Due to the fact the muscular fatigue decreases the neural
transmission velocity(21), maybe the ability in
creating efficient compensatory contractions around the joint is
reduced, resulting in a loss of the NMC and higher changes in the
joint positioning. But this is only a speculative statement, as
the aim of the study was not to analyze any difference in the
balance and posture of the individuals.

The present study has identified a significant increase in the
TMR in individuals after inducing the muscular fatigue. The
latency period of the fibularis muscles was similar to those
found in the literature. Some authors(14,35) have
presented studies assessing the TMR of the fibularis on sudden
inversion boards in individuals with stable and unstable ankles,
and the values found had a significant variation. The time of the
fibular reaction may be influenced by some factors. Studies
testing the reliability of those measurements assessed 30
individuals, and it was verified that the time of the fibular
reaction did not present a statistically different result between
both genders and the left and right limbs, and it was found no
influence of the body weight; there was a decrease in the
pre-warming period and an increase after the fatigue, and it
decreased with a 15º plantar flexion. The tests
performed in different days and times did not show any
difference; so, the authors have concluded that the time of the
fibular reaction is a reliable measurement(35). In the
present study, it was chosen the right limb, and the tests were
performed in three days in the same hour.

Other factors that have influenced the results of such type of
measurement were: the platform angle and the criterion for the
muscular activation (CMA). The angle used on the platform in this
study was 20o(29); nevertheless, other studies used
18º to 35º angles(14,35,36). It
is quite probable that the different angles lead to different
afferences, and this would cause different motor responses.

As to the beginning of the muscular activation, normally, it
is used criteria such as: to consider the first electrical
activity of the muscle(29,35), or to calculate the
mean of the resting signal plus n times more the
SD(14,22,30).

The works using as criterion the activation of the first
muscular response after the stimulus have shown lower reaction
times. As to the other criterion used, it varied from 2 to 10x of
the SD(22) between authors. That difference may led
some researchers to consider the mean latency signal or even the
long latency as the first response of the muscle(14).
This may have occurred in the present study because it has used a
CMA of: [mean + (3xSD)]. When it is used three deviations above
the mean, it presents a 99.7% chance to consider a different
activity than the resting(31).

It is a consensus that the intact afferent nervous system is
important to provide the necessary feedback for an effective
motor control(11). Parallel to this, studies have
shown that the human proprioception is deteriorated by the
fatigue(16,18,19,33,34), and theoretically, this would
be one of the causes for the worsening in the motor responses.
According to the present study, it is known that the
proprioception contributes for the muscular reflection, thus
providing the dynamic joint stability(18). So, some
authors have suggested that the muscular fatigue would not have
apparent effects on the sense of the joint movement
(kinesthesia)(18). Despite the importance of the
feedback that comes from mechanoreceptors and the
proprioception(11,14), it is probable that the
muscular receptors have a major interference on the TMR, since it
was measured under a sudden perturbation and high velocity
condition, when the responsible by the defense mechanism was the
muscular fuse activated by the straining
reflection(8,37). In another study(14), it
was performed an anesthetic blockage of the ligament receptors of
the ankle, and it was seen that the fibular reaction to the
sudden inversion did not change (80/83 ms). These findings
suggest that the afferent information to the sensor-motor
capabilities were mediated by the receptors in the myotendinous
system.

Another process that may be involved is the recurrent
inhibition(38). The recurrent inhibition is a local
feedback circuit that can modify the reflective responses by
means of an interneuron known as Renshaw cell. This cell can be
activated by a supraspinal impulse, by the group III and IV
muscular afferents, and by a collateral branch of the axon of the
alpha-motoneuron (MN). The activation of the recurrent inhibition
results in a decrease in the excitability of the MN that can be
increased during the contractions in the fatigue state. Besides
the effects on the alpha-MN, such inhibition also generates
potential post-synaptics in the gamma-MN. This connection means
that the recurrent inhibition can modulate the muscular fuse
excitability and influence the relationship between the afference
and efference to the straining reflection(8). Some
authors(39) assessed the M1 and the muscular rigidity
interaction with their influences in the pre- and
post-performance in a marathon. The test protocol included
several jumping in an ergonometer. The interpretation in the
sensitivity of the reflection was based on measurements of the
patellar reflections and the M1. The fatigue has provoked a
considerable worsening of the neuromuscular function. The results
have shown a clear deterioration in the reflection sensitivity
after the fatigue, and they suggest that the modulation of the
neural input to the muscle has at least partial reflective origin
in the contracted muscles, and the decreasing muscular rigidity
that followed the decreasing reflection sensitivity, and such
lower rigidity may have been partially responsible by the weaker
muscular performance, due to the worse utilization of the elastic
power(39). According to the results found in the
present paper, the neuromuscular control is partially compromised
with the fatigue onset, and this can be a predisposing factor to
injuries. There are few available studies in the literature
aiming the relationship between the fatigue and
TMR(3,21,22).

CONCLUSION

The results attained in the present study must be carefully
interpreted. The conclusions must be accepted in the environment
in which the data was collected rather than in a generic way.
Thus, the muscular fatigue induced through resisted active
exercises did not influence the resting electrical signal of the
fibularis. There was a statistically significant increase in the
time of the muscular reaction after induction the fatigue,
showing that there is a neuromuscular compromise.

FUTURE
GUIDANCE

It is necessary to be very careful both in the sports and in
the daily activities for the muscular fatigue not be a possible
cause for injuries. To avoid tasks that demand extremely fast
muscular responses when the body presents signals it is tired
could be the ideal situation to prevent injuries. Along the
rehabilitation process, the precaution must be even higher,
because individuals who are in such situation probably present
proprioceptive and/or muscular deficits. Along the rehabilitation
sessions, it would be advisable to perform tasks that would need
an accurate neuromuscular control before exercising the required
muscles in order to prevent an injury worsening or recurrence.
Therefore, the training aiming the muscular resistance is very
important both to athletes and patients, since those muscles with
an increased resistance to the fatigue would expose in a lower
level individuals to muscle-skeletal injuries. Future studies,
besides of analyzing the time of the muscle reaction, must check
the effects of the muscular fatigue in the magnitude of its
strength and the duration of these effects.

THANKFULNESS

To our family:
parents, brothers, spouses and daughter. To our friends and colleagues: Feliciano
Bastos Neto and João Paulo Cañeiro for their support and help.
To the Director of the Laboratory of the Exercise Research (LAPEX) of the Rio
Grande do Sul Federal University (UFRGS)  Professor Doctor Antonio Carlos
Stringhini Guimarães and Professor Doctor Flávia Meyer by their
support.

All the authors declared there is not any potential
conflict of interests regarding this article.